Rebecca J. Lewis

Bimorphism in Male Verreaux’s Sifaka in the Kirindy Forest of Madagascar

Male primates in species with pronounced secondary sexual adornments can exhibit reversible or irreversible bimorphism, i.e., striking variation in the degree to which males express the adornments. Verreaux’s sifaka (Propithecus verreauxi verreauxi) use scent marking as a form of communication and exhibit sex differences in scent glands. Some males exhibit a pronounced brown staining around their sternal gland, whereas others do not. We studied morphological and behavioral characteristics of males in 6 social groups in Kirindy Forest, Madagascar, from November 2000 to March 2002 to evaluate the hypotheses that the bimorphism in male sifaka chest status represents alternative mating tactics and is a badge of status. Males are clearly divided into 2 categories: clean and stained chests, with rare, but informative, intermediate males. The chest staining probably results from the males scent marking with their sternal glands, because stained-chested males scent marked significantly more often than clean-chested males. Though sample sizes are small, chest status did not appear to depend on body size. Chest status is reversible and related to dominance rank. In each group, only 1 male, the dominant, was stained-chested, whereas all other (subordinate) males were clean-chested. These findings suggest that stained chests are visual and olfactory signals of dominance rank and that clean chests signal lack of competitive intent. Thus, this bimorphism may reflect alternative mating tactics used by males to maximize their reproductive success based upon their social environment.

Effects of the Distribution of Female Primates on the Number of Males

The spatiotemporal distribution of females is thought to drive variation in mating systems, and hence plays a central role in understanding animal behavior, ecology and evolution. Previous research has focused on investigating the links between female spatiotemporal distribution and the number of males in haplorhine primates. However, important questions remain concerning the importance of spatial cohesion, the generality of the pattern across haplorhine and strepsirrhine primates, and the consistency of previous findings given phylogenetic uncertainty. To address these issues, we examined how the spatiotemporal distribution of females influences the number of males in primate groups using an expanded comparative dataset and recent advances in Bayesian phylogenetic and statistical methods. Specifically, we investigated the effect of female distributional factors (female number, spatial cohesion, estrous synchrony, breeding season duration and breeding seasonality) on the number of males in primate groups. Using Bayesian approaches to control for uncertainty in phylogeny and the model of trait evolution, we found that the number of females exerted a strong influence on the number of males in primate groups. In a multiple regression model that controlled for female number, we found support for temporal effects, particularly involving female estrous synchrony: the number of males increases when females are more synchronously receptive. Similarly, the number of males increases in species with shorter birth seasons, suggesting that greater breeding seasonality makes defense of females more difficult for male primates. When comparing primate suborders, we found only weak evidence for differences in traits between haplorhines and strepsirrhines, and including suborder in the statistical models did not affect our conclusions or give compelling evidence for different effects in haplorhines and strepsirrhines. Collectively, these results demonstrate that male monopolization is driven primarily by the number of females in groups, and secondarily by synchrony of female reproduction within groups.

Effects of Habitat Light Intensity on Mammalian Eye Shape

Many aspects of mammalian visual anatomy vary with activity pattern, reflecting the divergent selective pressures imposed by low light and high light visual environments. However, ambient light intensity can also differ substantially between and within habitats due to differences in foliage density. We explored the effects of interhabitat and intrahabitat variation in light intensity on mammalian visual anatomy. Data on relative cornea size, activity pattern, and habitat type were collected from the literature for 209 terrestrial mammal species. In general, mammalian relative cornea size significantly varied by habitat type. In within‐order and across‐mammal analyses, diurnal and cathemeral mammals from forested habitats exhibited relatively larger corneas than species from more open habitats, reflecting an adaptation to increase visual sensitivity in forest species. However, in all analyses, we found no habitat‐type effect in nocturnal species, suggesting that nocturnal mammals may experience selection to maximize visual sensitivity across all habitats. We also examined whether vertical strata usage affected relative cornea size in anthropoid primates. In most analyses, species occupying lower levels of forests and woodlands did not exhibit relatively larger corneas than species utilizing higher levels. Thus, unlike differences in intensity between habitat types, differences in light intensity between vertical forest strata do not appear to exert a strong selective pressure on visual morphology. These results suggest that terrestrial mammal visual systems reflect specializations for habitat variation in light intensity, and that habitat type as well as activity pattern have influenced mammalian visual evolution. Anat Rec, 2011.

Social Influences on Group Membership in Propithecus verreauxi verreauxi

The size and composition of a social group can influence the reproductive success of its members. I examined the hypothesis that residents actively try to manipulate group size and composition in Verreaux’s sifaka (Propithecus verreauxi verreauxi). I collected behavioral data from 21 individuals in 5 social groups from November 2000 to March 2002 in the Kirindy Forest (C.F.P.F.) of western Madagascar. I investigated the affiliative and agonistic behaviors of resident males and females toward other group members to determine whether residents attempt to manipulate the costs and benefits of group membership. I also examined 3 cases of immigration attempts and 1 case of emigration. As expected, group members facilitated the residency of subordinate members of the opposite sex. For example, females sought out the subordinate males, responded to their calls, and even groomed them more. However, intrasexual relationships were also important for establishing or maintaining residency. The data, in conjunction with the observations of immigration and emigration events, suggest that resident individuals of both sexes attempt to influence group size and composition. I suggest that single–male groups are not the norm in Propithecus verreauxi verreauxi because females encourage, and males do not discourage, multiple males to reside in the group to increase group stability and to reduce the risk of infanticide.

Chest staining variation as a signal of testosterone levels in male Verreaux's Sifaka.

Male Verreauxs sifaka (Propithecus verreauxi) exhibit variation in the staining of chest hair in association with the activity of the sternal gland. Scent-marking behavior and social relationships have been shown to vary with the state of chest staining. Research on other mammals suggests that sternal gland activity is modulated by testosterone. The goal of this study was to examine the relationship among fecal testosterone, testes mass, and chest staining in sifaka. I predicted that for sifaka (1) testosterone and testes mass are positively correlated, (2) stained males have higher testosterone and larger testes than clean-chested males, (3) testes mass is greater during the mating season than the birth season, and (4) testes mass is comparable to species with multimale mating systems. Eighty fecal samples were collected from eight adult males in five social groups in the Kirindy Mitea National Park of Madagascar during the mating season and analyzed using enzyme immunoassays. Males were captured during the mating season and the subsequent birth season to measure body mass and testes size and to document chest staining. Stained males had significantly higher fT and larger testes mass than clean-chested males. Testes mass was significantly greater during the mating season than the birth season for all males. However, the stained males exhibited less testes mass reduction during birth season than clean-chested males. These results suggest that the activity of the sternal gland is regulated by testosterone and that sexual selection has shaped male morphological variation in Verreauxs sifaka.

Hierarchical social networks shape gut microbial composition in wild Verreaux's sifaka

In wild primates, social behaviour influences exposure to environmentally acquired and directly transmitted microorganisms. Prior studies indicate that gut microbiota reflect pairwise social interactions among chimpanzee and baboon hosts. Here, we demonstrate that higher-order social network structure—beyond just pairwise interactions—drives gut bacterial composition in wild lemurs, which live in smaller and more cohesive groups than previously studied anthropoid species. Using 16S rRNA gene sequencing and social network analysis of grooming contacts, we estimate the relative impacts of hierarchical (i.e. multilevel) social structure, individual demographic traits, diet, scent-marking, and habitat overlap on bacteria acquisition in a wild population of Verreauxs sifaka (Propithecus verreauxi) consisting of seven social groups. We show that social group membership is clearly reflected in the microbiomes of individual sifaka, and that social groups with denser grooming networks have more homogeneous gut microbial compositions. Within social groups, adults, more gregarious individuals, and individuals that scent-mark frequently harbour the greatest microbial diversity. Thus, the community structure of wild lemurs governs symbiotic relationships by constraining transmission between hosts and partitioning environmental exposure to microorganisms. This social cultivation of mutualistic gut flora may be an evolutionary benefit of tight-knit group living.

Grooming patterns in Verreaux's sifaka.

Lemur grooming has received very little attention in the literature. Nevertheless, allogrooming in lemurs has been suggested to be fundamentally different from the grooming of anthropoids. One reason is that lemurs generally rely on oral rather than manual grooming. Lemur allogrooming has also been suggested to serve less of a social function than has been attributed to anthropoid grooming. I analyzed the allogrooming behaviors of 29 Verreauxs sifaka (Propithecus verreauxi) living in five social groups in the Kirindy Forest of Madagascar. Based upon 1,586 observation hours, I found that sifaka, like anthropoids, spend very little time mutual grooming (2±3%). Half of all allogrooming involved parts of the body that could have been easily groomed by the recipient, such as the limbs. Even though ectoparasite loads are expected to be greater during the rainy season, allogrooming did not increase during the rainy season. Allogrooming rates were influenced by both rank and sex, and increased by 50–100% during the mating season. The results of this study suggest that allogrooming in Verreauxs sifaka plays an important social function, even though it is performed with a toothcomb. Am. J. Primatol. 72:254–261, 2010.

Group benefit associated with polymorphic trichromacy in a Malagasy primate (Propithecus verreauxi)

In some primate lineages, polymorphisms in the X-linked M/LWS opsin gene have produced intraspecific variation in color vision. In these species, heterozygous females exhibit trichromacy, while males and homozygous females exhibit dichromacy. The evolutionary persistence of these polymorphisms suggests that balancing selection maintains color vision variation, possibly through a ‘trichromat advantage’ in detecting yellow/orange/red foods against foliage. We identified genetic evidence of polymorphic trichromacy in a population of Verreaux’s sifaka (Propithecus verreauxi) at Kirindy Mitea National Park in Madagascar, and explored effects of color vision on reproductive success and feeding behavior using nine years of morphological, demographic, and feeding data. We found that trichromats and dichromats residing in social groups with trichromats exhibit higher body mass indices than individuals in dichromat-only groups. Additionally, individuals in a trichromat social group devoted significantly more time to fruit feeding and had longer fruit feeding bouts than individuals in dichromat-only groups. We hypothesize that, due to small, cohesive sifaka social groups, a trichromat advantage in detecting productive fruit patches during the energetically stressful dry season also benefits dichromats in a trichromat’s group. Our results offer the first support for the ‘mutual benefit of association’ hypothesis regarding the maintenance of polymorphic trichromacy in primates.

Patterns of male dispersal in Verreaux's sifaka (Propithecus verreauxi) at Kirindy Mitea National Park

Males of many group‐living mammals emigrate from their social groups to improve mating opportunities. To help mitigate the social and locational costs of dispersal and to increase reproductive benefits, they may immigrate seasonally, immigrate alongside a partner, and/or replace the alpha male (versus entering a group as a subordinate). Verreauxs sifaka (Propithecus verreauxi) are highly seasonally breeding primates characterized by male‐biased dispersal. We hypothesized that (i) males time immigrations to pursue immediate mating opportunities, (ii) entrances with partners more often result in alpha male replacement, and (iii) male competitive ability affects immigration strategy and alpha male tenure length. To assess these proximate aspects of male dispersal, we examined 7 years of demographic, morphological, and behavioral data for five social groups of Verreauxs sifaka in the Kirindy Mitea National Park in western Madagascar. Contrary to expectations and studies of sifaka dispersal in other populations, we detected no strong seasonal pattern in immigrations. Immigrations occurred individually and with partners, and a trend existed for partners to increase the likelihood of replacing an alpha male. Pronounced activity of the sternal scent gland (a proxy for testosterone and prior dominance status), but not body mass, canine size, or potential correlates of leaping ability, significantly influenced immigration strategy. The absence of a seasonal immigration pattern suggests that fluid group boundaries may allow mating success without establishment in a social group before the mating season. Our results also suggest that male immigration strategies are affected by age, prior dominance status, and testosterone levels but not morphological indicators of individual competitive ability. Coalitions may be used to improve competitive ability. Finally, differences in seasonal immigration patterns and length of alpha male vacancies observed at Kirindy Mitea may be due to the relatively low population density. Am. J. Primatol. 79:e22455, 2017.

Noninvasive molecular sexing: An evaluation and validation of the SRY‐ and amelogenin‐based method in three new lemur species

Many lemur species are arboreal, elusive, and/or nocturnal and are consequently difficult to approach, observe and catch. In addition, most of them are endangered. For these reasons, non-invasive sampling is especially useful in primates including lemurs. A key issue in conservation and ecological studies is to identify the sex of the sampled individuals to investigate sex-biased dispersal, parentage, social organization and population sex ratio. Several molecular tests of sex are available in apes and monkeys, but only a handful of them work in the lemuriform clade. Among these tests, the coamplification of the SRY gene with the amelogenin X gene using strepsirhine-specific X primers seems particularly promising, but the reliability and validity of this sexing test have not been properly assessed yet. In this study, we (i) show that this molecular sexing test works on three additional lemur species (Microcebus tavaratra, Propithecus coronatus and P. verreauxi) from two previously untested genera and one previously untested family, suggesting that these markers are likely to be universal among lemurs and other strepsirrhines; (ii) provide the first evidence that this PCR-based sexing test works on degraded DNA obtained from noninvasive samples; (iii) validate the approach using a large number of known-sex individuals and a multiple-tubes approach, and show that mismatches between the field sex and the final molecular consensus sex occur in less than 10% of all the samples and that most of these mismatches were likely linked to incorrect sex determinations in the field rather than genotyping errors.